The not-so-Dark Ages: Ecology for human growth in medieval and

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 000:000–000 (2008)
The Not-So-Dark Ages: Ecology for Human Growth in
Medieval and Early Twentieth Century Portugal as
Inferred From Skeletal Growth Profiles
Hugo F.V. Cardoso1,2* and Susana Garcia3
1
Departamento de Antropologia & Centro de Investigação em Antropologia e Saúde, Universidade de Coimbra,
3000-056 Coimbra, Portugal
2
Faculdade de Medicina, Universidade do Porto, 4200-319 Porto, Portugal
3
Instituto Superior de Ciências Sociais e Polı́ticas & Centro de Administração e Polı́ticas Públicas,
Universidade Técnica de Lisboa, Pólo Universitário do Alto da Ajuda, 1300-663 Lisboa, Portugal
KEY WORDS
growth patterns; child labor; urbanization; industrialization; living conditions
ABSTRACT
This study attempts to address the issue
of relative living standards in Portuguese medieval and
early 20th century periods. Since the growth of children
provides a good measure of environmental quality for
the overall population, the skeletal growth profiles of
medieval Leiria and early 20th century Lisbon were
compared. Results show that growth in femur length of
medieval children did not differ significantly from that of
early 20th century children, but after puberty medieval
adolescents seem to have recovered, as they have significantly longer femora as adults. This is suggestive of
greater potential for catch-up growth in medieval adolescents. We suggest that this results from distinct child
labor practices, which impact differentially on the
growth of Leiria and Lisbon adolescents. Work for medieval children and adolescents were related to family activ-
ities, and care and attention were provided by family
members. Conversely, in early 20th century Lisbon children were more often sent to factories at around 12 years
of age as an extra source of family income, where they
were exploited for their labor. Since medieval and early
20th century children were stunted at an early age,
greater potential for catch-up growth in medieval adolescents results from exhausting work being added
to modern adolescent’s burdens of disease and poor
diet, when they entered the labor market. Although
early 20th century Lisbon did not differ in overall unfavorable living conditions from medieval Leiria, after puberty different child labor practices may have placed
modern adolescents at greater risk of undernutrition
and poor growth. Am J Phys Anthropol 000:000–000,
2008. V 2008 Wiley-Liss, Inc.
There is a European traditional view of history which
depicts the medieval period as the ‘‘Dark Ages.’’ The concept seems to have been created because the Middle
Ages have been seen as a religiously dominated period of
social decline, antiscience, and of brutish and miserable
peasant life, although historians and archaeologists have
done much to discredit such image. However, could the
Middle Ages have been more detrimental for human
health than the unhygienic and overcrowded conditions
and spread of communicable diseases, brought about by
increased urbanization and industrialization of the 19th
and 20th century? Industrialization has embodied the
notion of progress, characterized by unprecedented economic growth, the factory system of production based on
artificially powered machines, and by the ability to produce more than was needed to sustain a large percentage of the population. Yet, living conditions during the
Industrial Revolution deteriorated for a large percentage
of the population, socioeconomic disparities increased,
and people were at greater risk of malnutrition and
infection. Evidence has accumulated that living conditions of Europeans actually declined progressively from
the late Middle Ages to the early industrial revolution
(Lewis, 2002; de Beer, 2004; Steckel, 2004; KemkesGrottenthaler, 2005; Maat, 2005).
The main source of evidence for such a change in living conditions since the Middle Ages is past human stature and growth patterns reconstructed from skeletal
remains in bioarchaeological studies. The use of growth
and stature data to infer variations in the standard of
living relies on the assumption that the rate of growth of
the individuals of any population and their final attained
height reflect sanitary conditions, nutritional quality,
amount of energy expenditure, and overall health during
childhood (Tanner, 1982; Susanne, 1984; Fogel, 1986;
Schell, 1989; Bogin, 1999; Mays, 1999). The Middle Ages
have also been traditionally viewed as a particularly difficult period for children and childhood. This view has
been brought about largely by the influence of Ariès
(1962). According to Ariès, medieval children were
largely ignored and were viewed as, essentially, small
and inadequate adults. Children’s lives were perilous,
C 2008
V
WILEY-LISS, INC.
C
Grant sponsor: Fundação para a Ciência e Tecnologia, Portugal;
Grant number: SFRH/BPD/22142/2005.
*Correspondence to: Hugo F.V. Cardoso, Departamento de Antropologia, Universidade de Coimbra, Rua do Arco da Traição, 3000056 Coimbra, Portugal. E-mail: [email protected]
Received 14 November 2007; accepted 26 March 2008
DOI 10.1002/ajpa.20910
Published online in Wiley InterScience
(www.interscience.wiley.com).
2
H.F.V. CARDOSO AND S. GARCIA
TABLE 1. Breakdown of the Leiria and Lisbon samples by age group and distribution of individuals in the Lisbon
sample by decade of birth
Lisbon
Age groups
0.0–0.9 years
1.0–4.9 years
5.0–12.9 years
Total (subadults)
18.0–29.0 years
30.0–49.0 years
[50.0 years
Total (adults)
Leiria
1900–1909
1910–1919
1920–1929
1930–1939
1940–1949
1950–1959
[1959
Total
5
6
14
25
10
23
14
47
–
2
2
4
18
26
8
52
2
1
2
5
6
6
10
22
2
7
9
18
14
6
–
20
–
4
2
6
7
4
–
11
1
6
6
13
6
–
–
6
3
12
6
21
–
–
–
–
1
–
–
1
–
–
–
–
9
32
27
68
51
42
18
111
rough, and hard, where disease, poor diet, and neglect
took their toll. Although Ariès’ theory has been disputed
by social historians (e.g., Shahar, 1990; Oliveira, 2007)
over the years, the only study which actually provides
direct evidence for a decline in childhood health from the
medieval to the early industrial period is Lewis (2002).
In this study, subadult skeletons from medieval and
post-medieval English archaeological sites were compared and it was found that the industrial London sample showed retarded growth, higher levels of stress, and
a greater prevalence of metabolic and infectious disease
compared with the rural and urban medieval samples.
Comparing the growth rate between two, or more,
archaeological samples of immature skeletal remains
involves the construction of a skeletal growth profile
(SGP) to examine the cross-sectional age-progressive
trend in growth (Hoppa, 2000). In SGPs, a proxy for
statural growth such as a long bone measurement, usually femur length, is plotted against a measure of chronological age, such as dental age. The basic assumption
is that dental development is less sensitive to environmental insults and thus considered the best indicator of
chronological age, whereas skeletal development is more
affected and thus provides a measure of growth faltering
and health differentials (Saunders et al., 1993; Hoppa,
1992, 2000; Cardoso, 2007a). Under stressed environmental conditions, a large number of individuals will
show a bone growth deficit relative to dental age, and
this relative difference indicates a delay in skeletal
growth which has been interpreted as the result of environmental effects. The demonstration of differential
growth between samples is used as evidence for differential health status between entire populations, either
temporally or geographically (Johnston and Zimmer,
1989; Saunders, 1992, 2000).
This study addresses the question of whether the Portuguese Middle Ages were a period of miserable living conditions when compared with the period of increased urbanization associated with industrialization. This was carried
out by comparing the skeletal growth profile of a sample
of children from a late medieval cemetery in Leiria with
that of a sample of identified subadult skeletal material
from early 20th century industrial Lisbon. Although Portugal experienced a late and incipient industrial revolution, the city of Lisbon supported a large services sector
and small industries of traditional and manufacture level,
and the urban growth of the city was greatest during the
first half of the 20th century, because of migration movements of poor rural people who fled their home town in
search of jobs and a better standard of living. The expectation is to detect greater deficits in the growth of early
American Journal of Physical Anthropology
20th century children as a result of poor health and living
conditions, malnutrition and greater socioeconomic disparities associated with increased urbanization and industrialization, in spite of the supposed lower standard of living
during the Middle Ages. Although the samples are separated by over 500 years of history, there are no reasons to
believe that genetic factors play a significant role in
growth differences.
MATERIALS AND METHODS
The samples
Two samples of subadult skeletons were chosen for
their sizes, good overall state of preservation, and contrasting population types. The late medieval sample utilized comprises the skeletal remains of 157 individuals,
excavated from the urban medieval churchyard associated with the São Martinho Church in Leiria, central
Portugal. This church was built around 1211 and
destroyed between 1549 and 1553 (Gomes, 1990). Presumably, the burials, which have been excavated from
this cemetery, date to this period of time. The 1211–1553
chronology was subsequently confirmed by archaeological findings (e.g., coins) and radiocarbon analysis
(Garcia, 2007). During the excavation, a considerable
amount of disarticulated skeletal material was recovered, but only fully articulated skeletons, representing
single complete burials, were analyzed. Because of preservation, only 47 adult (18 females and 29 males) and
25 subadult skeletons were used in this study. Only
skeletons whose dental age has been estimated above
18 years and whose long bones showed complete epiphyseal union were included in the adult segment of the
Leiria sample. A breakdown of the Leiria sample by age
groups can be seen in Table 1. The Leiria subadults
were retrieved from the same cemetery as the adults
and no separate area for their burial was identified during the excavation. Additionally, no preferential treatment was given to child burials. Historical documents
also point to a very heterogeneous population in the São
Martinho area, with all social classes being represented,
including members of the local aristocracy (Gomes,
1990).
The Leiria series typifies the urban medieval period in
Portugal, contemporaneous with the establishment and
consolidation of the kingdom of Portugal (1143) and later
with the early Age of Discoveries. Despite the occasional
famine outbreak and armed conflict, particularly with the
neighboring kingdom of Castela, the Portuguese Middle
HUMAN GROWTH IN MEDIEVAL AND EARLY 20TH CENTURY
Ages were a period of territorial stability and relative economic efficiency given the country’s isolation (Magalhães,
1993; Mattoso, 1993). Leiria, in particular, seems to have
been a relatively prosperous town during the Middle Ages.
It was very dynamic commercially and many service sector activities were established there, particularly in the
area surrounding the São Martinho church. An indication
of Leiria’s prosperity is house rent prices in the main
streets, which were considerably high compared with
those of other medieval Portuguese towns and cities,
including the capital city Lisbon (Gomes, 1990). Besides
its commercial activity, this town area was also very
attractive due to the proximity of a permanent water
source, the Lis River. The land around Leiria was and still
is one of the richest in the country, which was the basis of
its agricultural production and overall prosperity. Greater
agricultural production, easy access to water sources, and
wider distribution of goods must have contributed to
improved medieval diets of the Leiria people. Medieval
historians suggest that medieval diet was both diverse
and rich in fresh products (Gonçalves, 2004). The exact
size of the Leiria population during this period is
unknown, but several indirect sources point to increasing
numbers between 1200 and 1500. Rural migration was
particularly intense after the Black Plague of 1348/1349
when there was a high demand for manual labor in urban
areas. Around the year 1700, the population size of Leiria
was documented as 3,500 souls (Lima, 1736). Considering
that Leiria was an important Portuguese medieval town,
the best guess for the population size of Leiria during the
Middle Ages, would be between 1000 and 3000.
The Lisbon collection represents the early 20th century densely urbanized/industrial sample and it comprises a series of approximately 700 fully identified skeletons obtained from public cemeteries in the Lisbon area
between 1981 and 2003 (Cardoso, 2006). A total of 68
subadult and 111 adult (53 females and 58 males) skeletons were utilized. Given the wide interval of years of
birth in the collection (1805–1972) and to control for
potential secular trend effects on stature, the adults and
subadults were selected to insure that they did not
belong to different birth cohorts. Although the adult and
subadult segments of the Lisbon sample are not entirely
of the same birth cohorts, the distribution of birth years
do not show any significant differences (v2 5 3.51, P \
0.74, df 5 6), with the majority of birth dates falling
between 1900 and 1950. Table 1 shows the distribution
of individuals in the Lisbon sample by age group and
birth decade.
The Lisbon children embody the increased urbanization and industrialization of the Portugal’s capital city
during the early republican and dictatorship years.
Established as a republic state in 1910, Portugal experienced civil unrest until the rise of a dictatorship in 1933.
It was not until 1974, with a military coup, that the shift
from a dictatorial government to a democratic pluralist
political system took place. As Portugal’s capital city, Lisbon witnessed and experienced the most important political events and economical developments. Portugal
emerged from the 19th century as a declining world political power, with a fragile agricultural system, incomplete industrialization, a weak capitalist system, and a
centralized and strong catholic church. During most of
the dictatorship years, Portugal remained a very isolated, underdeveloped and traditional society, where
social and economic conditions of the late 19th century
largely prevailed. The majority of farmers were still
3
practicing subsistence agriculture with little motivation
for the establishment of industrial and capitalist economies (Giner, 1982). During the 20th century, the
decrease in the population working in the primary sector
was not so much a consequence of increased productivity
in the secondary sectors, but of increased migration to
urban centers and employment in the tertiary sector
(Maia, 2001). Only the major urban centers, such as Lisbon, had significant industries, but the majority of them
were small and of traditional sectors. The industrial
labor force was also predominantly illiterate, with few or
no technical skills, supported by women and child work
and with no free association rights. The Lisbon area was
the region of greatest population growth in absolute
terms. On one hand, being the country’s capital, it
housed much of the governmental institutions, and on
the other, it also comprised the most important manufacturing and service sector jobs. The city’s population
increased roughly threefold between 1890 and 1960,
from approximately 300,000 inhabitants to more than
800,000 (Baptista and Rodrigues, 1995). Lisbon, however, was one of the Portuguese cities with the lowest
birth rates, and urban growth was accomplished almost
solely at the expense of rural migration (Paúl, 1945).
Data collection and analysis
To compare growth status of the Leiria children with
that of the Lisbon children, cross-sectional skeletal
growth profiles (SGP) were constructed for each sample,
using growth in femur length as a measure of statural
growth and growth in tooth length as a measure of age.
Tooth length was chosen as the estimate of age because
progression in tooth calcification is considered the single
best estimator of true chronological age. Tooth length
was measured according to the recommendations of
Liversidge et al. for use in age prediction (Liversidge
et al., 1993; Liversidge and Molleson, 1999), as the distance from the cusp-tip to the developing edge of crown
or root in the midline, parallel to the long axis of the
tooth. In teeth with more than one cusp or root, the
maximum length was measured. All available mandibular deciduous and permanent teeth were measured to
the nearest tenth of a millimeter using a digital sliding
caliper. In the Leiria sample, only loose teeth were measured and in the Lisbon sample, approximately half of
the tooth measurements were obtained from periapical
radiographs. Tooth length was measured on the left side
only or on the right side if the left was unavailable. Radiographs in the Lisbon sample were taken in relation to
the lingual-buccal plane with the aid of an extension
cone paralleling film-holding instrument and with a 10
mm metal bar attached to the specimen to provide a
gauge to assess image magnification. Because tooth
length measured on radiographs is used as a surrogate
for actual tooth length in the Lisbon sample, it was important to assess whether the two measurements differ
significantly. Twenty isolated uniradicular deciduous and
permanent teeth, six isolated multiradicular deciduous
teeth, and twenty isolated multiradicular permanent
teeth were measured directly and then replaced in their
sockets, where they were radiographed. Differences
between direct and radiographic measurements were
compared using a paired t-test or a Wilcoxon paired-sample test (when comparing multiradicular deciduous
teeth) and were never found to be significant (P [ 0.10)
(see also Cardoso, 2007b).
American Journal of Physical Anthropology
4
H.F.V. CARDOSO AND S. GARCIA
Femur length provides a simple cumulative measure
of physical growth in skeletal samples and since there is
a high correlation between stature and femur length
(0.8) (e.g., Pearson, 1899; Trotter and Gleser, 1952;
Ruff, 2007); it is considered a proxy for statural growth.
Maximum femur length in the adults and femur diaphyseal length in the subadults of both samples were
measured to the nearest whole millimeter using an
osteometric board. Left femora were measured with
replacement by the right if the left was unavailable or
poorly preserved. To insure comparability of data in
SGPs across the different age groups, only femora with
unfused proximal and distal epiphysis were measured.
Although epiphyseal union in the femur can occur
beyond the age of 13 years, our samples include preadolescent individuals only, selected on the basis of dental
age estimates as all skeletons below the age of 12.9 years.
Because sex cannot be easily determined in the unidentified prepubertal skeletons of the Leiria sample, samples
were pooled with regards to sex. Since most of the sex
differences in body size are due to the events of puberty
(Tanner, 1989; Bogin, 1999), pooling male and female
growth curves is not likely to increase significantly the
variation of the growth profiles, even if one sex outnumbers the other.
Two approaches were used to construct SGPs. In the
first approach, femur length was plotted against absolute
tooth lengths to construct the SGP and this enabled
growth comparisons between samples to be made tooth
by tooth (length) and not by an overall single dental age.
Because tooth length is a continuous variable, it avoided
unnecessary complications from building femur growth
profiles with tooth calcification stages, which are discrete
variables. In addition to tooth length being preferred relative to tooth formation stages, due to the latter being a
discrete trait and also subjected to higher subjectivity of
assessment, the greatest advantage of using absolute
tooth length is that femur growth occurs as a near-linear
function of tooth length. Visual inspection of the scatter
plots was the basis for establishing a near-linear relationship between femur length and tooth length, which
was subsequently confirmed when nonlinear regressions
were fitted to the data. Since each SGP is built tooth by
tooth, the relationship between femur length and the
length of any tooth represents a near-linear fraction of a
nonlinear relationship represented by the whole growth
period. In cross-sectional samples, the relationship
between femur length and dental age is approximately
linear between birth and 2 years of age and then
between 2 and 18 years.
Because teeth were considered individually, some
SGPs provided very small sample sizes, particularly
with the Leiria series. Consequently, some SGPs were
subsequently eliminated from the analysis, namely those
whose femur length was plotted against the deciduous
central incisor and the permanent third molar, second
premolar, and lateral incisor. Once femur diaphyseal
length was plotted against tooth length, simple linear
regression equations were fit to data points of each sample (Leiria and Lisbon) and compared. Since femur
growth occurs as a near-linear function of tooth length,
simple analysis of covariance (ANCOVA) was employed
to compare the slopes and elevations of the two samples’
regression lines. First the ANCOVA was carried out
including the interaction term between the covariate
(sample) and the independent variable (tooth length). If
statistically significant, the slopes were considered differAmerican Journal of Physical Anthropology
ent and the elevations could not be compared. If differences between slopes were nonsignificant, the interaction
term was removed and the ANCOVA rerun. If results
were statistically significant, the elevations were considered different. Differences between elevations are the basis for concluding differences in femur length between
samples. Because of small sample sizes in the Leiria
sample, after the ANCOVA was performed, the residuals
were examined for signs of non-normality in each SGP.
Normal probability plots approximated straight lines
and did not show significant departures from normality,
except with the first permanent molar. Homocedasticity
of Y variables for each SGP was also examined using
Levene’s test for equality of variances. Heterocedasticity
of femur length was only detected when age was estimated from the length of the deciduous canine.
In the second approach, femur length was plotted
against an overall mean dental age to construct the SGP
for each sample. Dental age was calculated for each skeleton as the mean age obtained from all available teeth
using Liversidge and coworkers’ prediction equations for
the deciduous (Liversidge et al., 1993) and permanent
dentition (Liversidge and Molleson, 1999). Given the
nonlinear relationship of dental age with femur length,
fourth-degree least-square polynomial regression equations were calculated for each sample and compared. A
polynomial analysis of covariance (ANCOVA) was
employed to compare the two samples. Similarly to the
previous approach, the homogeneity of covariate-dependent variable slopes was tested and if nonsignificant, the
analysis was rerun without the interaction term, after
which the growth curves were considered different if
statistically significant results were obtained. The
approach followed here is similar to that of Pinhasi et al.
(2005, 2006). Residuals in the second approach were
examined and did not show significant departures from
normality. Levene’s test for equality of variances also
demonstrated homocedasticity of the Y variable for each
SGP. All statistical analyses were performed with the
statistical package STATISTICA.
The Leiria and Lisbon samples were also compared
with a better nourished population to assess the amount
of growth deficit in both samples. This was achieved by
computing individual z-scores. Z-scores are calculated by
subtracting from every observed femur length the mean
of a reference sample and dividing by the standard deviation, for the appropriate age. The nineteenth century
church cemetery sample from Belleville, Ontario,
(Saunders et al., 1993) was chosen as the reference data,
since it has been shown to represent a well-nourished
population by comparison with the modern Denver
Growth Study data (Maresh, 1970). Because sex in the
Leiria sample is not known and the Lisbon subadults
are treated as if sex is also unknown, this archaeological
sample was also considered more suitable to calculate zscores, since it provides age appropriate femur length
data which are not sex-specific. Other than comparing
SGPs between the Leiria and Lisbon samples, differences in adult femur length between the two samples
were also compared via a t-test. This comparison was
carried out to demonstrate whether any differences in
size between samples in the preadolescent years are
passed on to the adults and evaluate possible differences
in growth during the adolescent years. The Lisbon and
Leiria adults were also compared with the Belleville
adults via a t-test to assess the amount of deficit in adult
femur length in both Portuguese samples.
5
HUMAN GROWTH IN MEDIEVAL AND EARLY 20TH CENTURY
TABLE 2. Comparison between Leiria (medieval) and Lisbon (early 20th century) regression coefficients when femur
diaphyseal length is regressed on tooth length
Leiria sample
Lisbon sample
Tooth
N
A
SE (A)
b
SE (b)
r2
SEE
N
A
SE (A)
b
SE (b)
r2
SEE
F
F0
m2
m1
C
i2
M2
M1
PM1
C
I1
5
4
6
5
7
6
5
11
8
29.53
52.39
48.19
38.79
160.09
127.58
117.29
130.05
110.05
14.20
5.34
2.28
4.78
5.01
9.21
11.45
10.98
22.97
15.13
6.54
8.09
8.21
9.89
6.74
11.03
8.28
7.98
3.65
1.17
0.20
0.57
0.45
0.70
0.89
0.82
1.40
0.80
0.91
0.99
0.98
0.99
0.95
0.97
0.91
0.82
6.23
1.51
2.89
5.29
5.90
7.13
8.90
14.49
27.80
10
7
26
26
33
36
42
54
50
7.66
46.87
64.23
39.85
163.67
90.17
148.48
111.96
89.89
11.92
11.34
5.32
6.66
6.95
7.72
6.32
5.63
6.05
18.46
8.65
6.99
8.45
10.02
9.98
9.73
9.79
9.82
2.24
2.38
0.46
0.58
0.58
0.69
0.51
0.41
0.44
0.88
0.70
0.90
0.90
0.90
0.86
0.90
0.92
0.91
8.16
6.00
10.43
12.65
16.15
16.25
20.01
21.37
18.76
0.45
0.22
1.85
0.03
0.01
3.85
0.42
1.50
2.38
2.94
1.58
1.34
0.24
0.60
0.10
2.88
0.01
0.85
Femur diaphyseal length is estimated from the equation: y 5 A 1 b 3 x. The standard errors (SE) of A and b, the standard error of
the estimate (SEE) for regression predictions and the coefficient of determination (r2) is shown. The homogeneity of the regression
slopes (F) and of the elevations (F0 ) is compared by analysis of covariance (ANCOVA). All differences are statistically insignificant
(P [ 0.05).
Because we wish to infer differences in size from differences in femur length, it is important to note that
populations may differ in femur length relative to stature (Ruff, 2002) or lower limb length relative to stature
(Bogin and Rios, 2003), and that there are also important changes in such proportions during growth
(Buschang, 1982; Bogin, 1999; Ruff, 2007). However, our
approach assumes that both samples do not differ genetically and that adult height potential and body proportions are approximately the same in both samples.
Although there is no available data that can show
whether body proportions have changed significantly in
Portugal over the past 800 years, any genetic contribution to the difference in absolute femur length and in femur length relative to stature, between medieval and
early 20th century Portuguese, is not possible to assess
given that there is no known basis for the genetic determination of body size and shape differences between
populations (Bogin et al., 2001). Several peoples (Roman,
Germanic, and Berber) occupied the modern Portuguese
territory before the 12th century, but Portugal maintained a remarkable stability since that period without
major population movements into the country until the
late 20th century, except perhaps, that of the slave trade
between the 15th and 18th centuries (Serrão, 1992).
Nonetheless, there is no evidence for a differential
genetic contribution from such population movements to
distinct areas of the country between the 12th and early
20th centuries, except for the southern region of Alentejo
(Beleza et al., 2006). In addition, any explanation for differences in size between the Leiria and Lisbon samples
that relies partially on such population movements,
which are very imprecise and imperfect measures of
genetic change at best, is not useful given the enormous
plasticity of human growth in response to environmental
change (Bogin et al., 2001; Bogin and Rios, 2003). For
example, contemporary Portuguese have showed a remarkable change in height over the last 40 years (Padez,
2003; Cardoso, 2008) comparable with what other populations experienced as a consequence of a positive secular trend. From military conscript data, which represent
the entire country, it was shown that the Portuguese
male population increased in stature about 8.93 cm
between 1904 and 2000, with the greatest gain occurring
since the 1960s and 1970s (Padez, 2003). A genetic explanation cannot account for the rapid height change in
such a little time. The reason for this change lies,
instead, in a collective of environmental factors, from
improved quantity and quality of nutrition, to lessening
of infectious diseases, which were triggered by political,
economical, and social changes, that increased family
incomes, provided easy access to better nutrition and
health care and sanitary living conditions (Padez, 2003;
Cardoso, 2008). On these grounds, we are also inferring
different environmental conditions between the medieval
and early 20th century samples if growth differences are
detected between them.
RESULTS
Compared with the nineteenth century sample from
Belleville, the Lisbon children show a mean growth deficit of 21.6 z-scores (SD 5 1.50), whereas the Leiria children show a mean growth deficit of 22.0 z-scores (SD 5
1.26). Although there is a tendency for Leiria to show
greater growth retardation, differences between the samples are not statistically significant (t 5 1.42; df 5 88; P
5 0.1554). Both samples, therefore, show a significant
growth deficit. Adult data also show a deficit in femur
length in the Leiria and Lisbon samples when compared
with the Belleville sample. When compared with the Belleville adults (females: mean 5 429.5 mm, SD 5 22.80;
males: mean 5 464.0, SD 5 22.76), only the Leiria
females do not show significantly shorter femora (t 5
0.93; df 5 111; P 5 0.3536), whereas Leiria males (t 5
2.78; df 5 149, P 5 0.0062), Lisbon females (t 5 5.59; df
5 146, P 5 0.0000) and males (t 5 6.21; df 5 178, P 5
0.0000), all show significantly reduced femur length.
Medieval Leiria adults, however, have significantly
longer femora than early 20th century Lisbon adults.
Mean maximum femur length is 424.2 mm (SD 5 18.54)
for Leiria females and 451.3 mm (SD 5 19.48) for Leiria
males, and 408.4 mm (SD 5 20.10) for Lisbon females
and 441.5 mm (SD 5 22.77) for Lisbon males. Both the
females (t 5 2.93; df 5 68; P 5 0.0046) and the males
(t 5 1.98; df 5 85; P 5 0.0504) differ significantly
between the two samples. Comparatively, when the
growth of children in both samples is contrasted, the
Leiria children are not significantly delayed or advanced
relative to the Lisbon children. Table 2 presents the
regression coefficients of the Leiria and Lisbon samples,
when femur length is regressed on tooth length, and the
ANCOVA test results. Data in Table 2 show homogeneity
of slopes and elevations in all SGPs at the 0.05 probability level. This means that the Leiria and Lisbon regression lines do not differ significantly, regardless of the
American Journal of Physical Anthropology
6
H.F.V. CARDOSO AND S. GARCIA
TABLE 3. Comparison between Leiria (medieval) and Lisbon (early 20th century) regression coefficients when femur
diaphyseal length is regressed on dental age
N
A
Leiria sample
25
73.57
Lisbon sample
68
77.29
SE (A)
b
SE (b)
c
SE (c)
d
SE (d)
e
SE (e)
r2
8.16
55.72
12.40
210.10
4.53
1.02
0.56
20.03
0.01
0.97
7.06
46.90
8.82
26.61
3.18
0.66
0.41
20.02
0.01
0.96
Femur diaphyseal length is estimated from a fourth degree polynomial: y 5 A 1 b 3 x 1 c 3 x 1 d 3 x 1 e 3 x . The standard
errors (SE) of the coefficients and the coefficient of determination (r2) are shown. The homogeneity of the regression coefficients (F
5 0.87; P 5 0.3833) and of the elevations (F0 5 1.70; P 5 0.0953) is compared by a polynomial analysis of covariance (ANCOVA).
2
Fig. 1. Data points and regression lines obtained from the
Leiria (medieval) and Lisbon (early 20th century) samples,
where femur diaphyseal length is regressed on deciduous lateral
incisor length.
tooth length utilized. Only at the 0.10 probability level
did one regression line differ between samples in the
slopes (first permanent molar) and one regression line
differed in the elevations (first permanent premolar).
When considering the standard error of the regression
estimates, they are almost always greater in the Lisbon
than in the Leiria sample, which is a reflection of less
variation being sampled in Leiria. As a result, the Lisbon regression lines include wider 95% confidence intervals, which encompass a large amount of the Leiria
regression 95% confidence bands. These results, however, strongly suggest that the Leiria and Lisbon children do not differ in growth status before puberty. The
polynomial ANCOVA results for the comparison between
the two samples’ overall SGPs using dental age (Table
3), confirm that growth of Leiria children is not significantly different from that of Lisbon children.
Figures 1–3 were chosen to illustrate the relationship
between femur growth and tooth length (age) in the Leiria and Lisbon samples. In all figures, there are no differences between samples when femur length is plotted
against age. Overall, there is only a small tendency for
the Leiria regression line to be drawn below the Lisbon
regression line. This may be suggestive of a growth deficit in the Leiria sample, but the ANCOVA results indicate otherwise. The various graphs of femur length
plotted against tooth length represent various individuals at different ages, from birth to around 12 years of
age. Some individuals had one tooth measured whereas
others had more than one and thus are represented in
American Journal of Physical Anthropology
3
4
Fig. 2. Data points and regression lines obtained from the
Leiria (medieval) and Lisbon (early 20th century) samples,
where femur diaphyseal length is regressed on permanent first
premolar length.
Fig. 3. Data points and regression lines obtained from the
Leiria (medieval) and Lisbon (early 20th century) samples,
where femur diaphyseal length is regressed on permanent second molar length.
more than one of the figures and regression equations.
Figure 4 illustrates the SGP when femur length is
regressed on dental age estimates, using the entire samples. Except during middle childhood, where the Leiria
regression line is drawn below the Lisbon regression
line, growth in the two samples does not seem to differ,
HUMAN GROWTH IN MEDIEVAL AND EARLY 20TH CENTURY
Fig. 4. Overall skeletal growth profiles of the Leiria (medieval) and Lisbon (early 20th century) samples, where femur diaphyseal length is plotted against dental age. The regression line
depicted represents a fourth-degree polynomial adjustment.
thus substantiating and strengthening the results
obtained with the femur length by individual tooth
SGPs. These data show that until 12 years of age, the
increase in femur length in the Lisbon and Leiria samples is quite similar. However, significantly greater femur length in the Leiria adults is strongly suggestive
of differences in growth between the samples during
adolescence.
DISCUSSION
Skeletal growth profiles
Five important methodological considerations have to
be made with respect to the observed pattern of growth
between the medieval and modern samples. First,
because age estimators are identical in both samples,
errors in dental age assessment cannot be an explanation for the observed results. Second, several authors
(Johnston, 1962; Buikstra and Cook, 1980; Wood et al.,
1992) have pointed out that growth patterns in skeletal
samples which do not represent the growth of normal,
healthy children, but instead would represent a deficit
relative to the population norm. However, given that neither sample is comprised of living children, this criticism
is unlikely to hold for explaining the observed similarities and/or differences. Third, although it can be argued
that a SGP built with estimated dental ages using each
entire sample would suffice to compare growth between
the Leiria and Lisbon samples, our goal was to present a
novel approach to comparing growth data. This new
approach takes advantage of the near-linear relationship
of femur with individual tooth length and can simplify
the statistical comparison between different samples.
The main limitation with this approach to growth in
skeletal samples is that because SGPs are constructed
tooth by tooth, they tend to decrease the available sample size significantly, thus creating difficulties in the
detection of statistically significant differences. Fourth,
although the sample sizes for the Leiria sample are
somewhat low, it represents one of the largest samples of
preadolescent skeletons from one single Portuguese
archaeological site. Accordingly, we offer a tentative first
analysis of growth differences between medieval and
7
early 20th century Portuguese populations and infer
changes in the environments for human growth. Last,
this study is, by necessity, cross-sectional in nature
and these are able to provide a lower level of evidence of
causation.
The expectation of greater growth deficit in early 20th
century Lisbon, as a consequence of poor living conditions compared with the Middle Ages, was partially met,
but only in adolescence. The late medieval children from
Leiria were found to be neither delayed nor advanced in
growth of femur length compared to the early 20th century children from Lisbon. When z-scores and SGPs are
compared between both samples, results show that,
although the Leiria subadults tend to show a slighter
deficit in growth, the difference is never statistically significant. Although some SGPs could not be compared
when built with the length of the deciduous central incisor or of the permanent third molar, second premolar,
and lateral incisor, there is an overall consistent pattern.
The various SGPs by tooth length represent different
children at various ages, from approximately birth to
12 years of age and, therefore, support the assertion that
growth status does not differ between samples from
infancy to late childhood. This pattern is strengthened
by the results of the second approach, where femur
length was plotted against an overall dental age. On the
other hand, the Leiria adults were found to have significantly longer femora than the Lisbon adults, which is
suggestive of a recovery in femur length during adolescence in medieval youths. Neither sample, however, can
be considered to represent optimal rates of growth as
both samples of children show significant growth deficits
compared with a nineteenth century better-nourished
population from North America (Saunders et al., 1993).
The primary factor leading to the overall reduced adult
femur length and, by implication, short adult stature, in
these two populations is the growth retardation already
present during childhood, as shown by the z-score values. Therefore, environmental circumstances during
childhood seem to have been unfavorable in both samples, but during adolescence conditions may have
changed placing Lisbon at greater disadvantage.
The difference observed between the adults and subadults of both samples could arise if the Lisbon sample
comprises a greater proportion of girls or the Leiria sample a greater proportion of boys. Given that the growth
of girls is more buffered against environmental insults
(Stinson, 1985) and that the Lisbon adults have shorter
femora than the Leiria adults, the Lisbon subadults can
appear similar in size to the Leiria subadults if they
comprise more girls than Leiria and hence show an overall pattern of growth which is less affected by poor living
conditions. However, in the Lisbon sample there is
actually only slightly more males than females, and in
the Leiria sample, there is no reason to suspect that one
sex would outnumber the other in such a way as to bias
the results. The results could be also explained if the
subadults and adults of the same sample come from different socioeconomic strata. If the Leiria subadults are
of lower socioeconomic status than the adults, this could
explain the difference between samples, given that the
adults and subadults of the Lisbon sample do not seem
to differ in their socioeconomic background, as inferred
from the documentary records. But, as far as the authors
are aware, there is no evidence for this differential socioeconomic representation. Even if the Leiria subadults
were of lower socioeconomic condition than the adults, it
American Journal of Physical Anthropology
8
H.F.V. CARDOSO AND S. GARCIA
would still lend support to the conclusion that the environment for growth was poorer in the early 20th century
than during the medieval period.
If we are left to conclude that the medieval period provided a better environment for human growth after puberty, what could explain the differences in growth during adolescence that can be inferred from comparing
both samples? At the simplest level, these differences
seem to indicate a greater potential for catch-up growth
in the Leiria adolescents. Catch-up growth during adolescence is a common phenomenon in developing countries where prolongation of the growth period can make
up for some of the earlier growth deficit (Satyanarayana
et al., 1980, 1989; Kulin et al., 1982; Tanner, 1986;
Golden, 1994; Martorell et al., 1994; Norgan, 2000; Coly
et al., 2006). However, the marked growth retardation
incurred in early childhood generally remains into adulthood. Stunting seems to be reduced if the environment
is improved or if there is no further decline of an already
unfavorable environment. If the medieval children from
Leiria show a greater potential for catch-up growth compared with the modern children from Lisbon, we can
conclude that a change in the environment must have
occurred around puberty, which has resulted in a deterioration of the Lisbon adolescents’ nutritional status,
compared with that of the Leiria adolescents. We have
already argued against a genetic explanation for differences in size between the two samples and suggest that
the plastic ability of humans to adjust to changes in the
environment is the likely cause of variability in human
growth patterns which explains the differences between
the samples.
Environments for human growth
For most of the early 20th century, prevailing social
and living conditions in Portugal were those of the late
19th century. Living conditions were particularly difficult for the poor and working classes in Lisbon (Crespo,
1990), where overcrowding and unsanitary environments
were generalized and health conditions were very poor.
For example, a 1950s study on housing of the working
class in Lisbon (Moreira, 1950) found that 43% of the
families had no piped water, 69% had no electric power,
and 81% had no toilet. Although, historically, the construction of piped sewerage systems were important for
improving urban public health, by 1970, 27% of the population in Lisbon still had no access to the public sewerage system (INE, 1970). It was only after the 1960s and
1970s that the Portuguese population experienced major
changes in exposure to, and treatment of, infectious disease, and in welfare (Sanches and Carvalho, 1983;
Carreira, 1996; Veiga et al., 2004). Therefore, given that
most individuals in the Lisbon sample were born
between 1900 and 1950, they did not experience these
recent environmental changes. Life in medieval Leiria
would also have shared the perils of a premodern epidemiological profile, where infectious disease prevailed.
Nonetheless, social support and health care was provided by various charity institutions of catholic inspiration who offered shelter, food, and some relief and medical assistance to the medieval poor of Leiria. The not so
needy would also have access to the services of several
professional health caretakers, such as physicians, surgeons and botanists (Gomes, 1999). People in Leiria also
benefited from living in a less densely populated urban
center, which provided some protection against aggraAmerican Journal of Physical Anthropology
vated sanitation problems and spread of communicable
diseases, compared to Lisbon.
Given that growth in height is considered a proxy for
long-term health and nutritional experience, as it
reflects the synergetic difference between the accumulated intake of nutrients and use of energy in work and
fighting infection (Floud, 1994; Steckel, 1995), it is
hypothesized that, since health conditions of Leiria and
Lisbon children were probably similar with respect to exposure to, and treatment of, infectious disease, differences in adolescent growth may have resulted from
changes in physical labor, which have a negative impact
on nutritional status. It is also unlikely that the disease
environment has changed from childhood to adolescence
in both samples, and thus it seems improbable that the
difference in growth status at adolescence between the
samples was caused by a differential decrease or
increase in exposure to infectious disease. We suggest
that it might have been the entering of Lisbon children
into the labor market which might have triggered the
environmental change responsible for reduced or absent
catch-up growth, namely increased physical activity and
risk of undernutrition. This rests on the notion that normal growth spurts during puberty and adolescence are
adversely affected by increased manual labor and, as a
consequence, by the poor nutrient intake which does not
compensate for the energy diverted from growth to physical work. Growth velocities, and hence nutrient needs,
are high during adolescence and, therefore, growth during this period is sensitive to a poor nutritional status
(Bogin, 1999). There is one study, carried out in Japan,
which demonstrates a difference of 4 cm in height
between those who began work before the age of 14 and
those who began after 18 years of age, whereas their
height had been comparable at age 12 (Mendelievich,
1979). Findings in other studies (Satyanarayana et al.,
1986; Hawamdeh and Spencer, 2001, 2003; Duyar and
Özener, 2005) indicate that working children are behind
in height when they are compared with their nonworking same-age peers living in similar conditions and
that these differences are carried on to adult life
(Satyanarayana et al., 1986; Duyar and Özener, 2005).
Findings in this study seem to suggest that when the
Lisbon children entered the labor market, at about
12 years of age (Valente, 1986; Campinho, 1995), their
net nutritional status may have decreased compared
with the Leiria children and thus may explain why the
potential for catch-up growth is lower or absent in
Lisbon. Physical work did not affect the body height per
se, as they were already stunted at infancy and childhood, but diminished the potential for recovery in height
during the adolescent years, by diverting available
energy in the diet away from growth. In Leiria, however,
net nutritional status seems to have allowed for some recovery in size by prolongation of the growth period. Historical data from Medieval and early 20th century Portugal seems to lend support to this hypothesis. In Lisbon,
a large percentage of the local industrial labor force was
comprised of children. In some industries, children made
up almost 25% of the work force (Rosas, 1994). Although
most factories and services admitted apprentices in their
facilities, these children and/or adolescents were frequently subjected to a harsh, heavy, and demanding
work environment, serving as unskilled work and
exploited for their labor (Cândido et al., 1965). These
children worked for meager salaries to help support
their poor families, who lived in unsanitary and crowded
HUMAN GROWTH IN MEDIEVAL AND EARLY 20TH CENTURY
living conditions in working class overpopulated neighborhoods (Rosas, 1994). It was only after the 1950s and
1960s that Portugal started to experience a transformation, with stricter child labor laws, and an overall
improvement in the standard of living. Comparatively,
medieval children were incorporated into rural work
from an early age, but provided supplementary labor
only to help support their families and were young
apprentices of a series of family activities, such as manufacture, crafts, and services (Oliveira, 2007). The conditions of children employed in family activities may have
been better, because the effort, fatigue, and dangers to
which they are frequently exposed are balanced in part
by the care and attention they receive from other family
members (Mendelievich, 1979). We are not implying that
the lives of Leiria adolescents were not harsh and perilous, but instead that they were not as difficult as the
lives of Lisbon adolescents, as reflected in their different
growth status.
Interestingly, Saunders et al. (1993) noticed a phenomenon similar to what we describe here. The Belleville SGP exhibit a relationship similar to the modern
Denver growth profile up to 12 years, but as adults the
Denver sample shows longer femora than the Belleville
sample. Saunders et al. (1993) suggest as a possible explanation that the Denver sample had an earlier and
longer adolescent growth, but they do not elaborate on
this any further. Since the prolongation of the growth period tends to reflect a compensation for an earlier growth
deficit (Satyanarayana et al., 1980, 1989; Kulin et al.,
1982; Tanner, 1986; Golden, 1994; Martorell et al., 1994;
Norgan, 2000; Coly et al., 2006), we would suggest,
instead, that the Denver sample simply had a greater
growth rate during adolescence. However, any environmental explanation for this difference would be purely
speculative, given our lack of knowledge about the details
of the historical and cultural context of the Belleville sample. Other results similar to those of this study have been
infrequently reported, with the exception of the works
carried out by Steckel (1986) and Lewis (2002). Using
records of African-American slave children anthropometrics, Steckel was able to show that slaves were severely
stunted (undernourished) as children, but when slaves
entered the labor force they caught-up, and became as
tall or as taller as their African adult counterparts.
Although net nutrition should have deteriorated for
slaves at this time, there was in fact an improvement in
the slave diet sufficient to offset the additional requirements of physical activity and to allow a small amount of
catch-up growth during adolescence. This remarkable pattern of growth and dietary recommendations of owners
supports Steckel’s assertion that slaves were poorly fed as
children but extraordinarily well fed as workers.
Although neither the Lisbon nor the Leiria children experienced similar changes in their diets, Steckel’s study
shows that such environmental modifications at puberty
can have tremendous effects on the growth of adolescents,
when compared with the children. With respect to the relative better environment for human growth of medieval
towns, Lewis (2002) found that early modern London children from Spitalfields were consistently shorter, showing
a difference of up to 3 cm in femur length than their
urban medieval counterparts from St. Helen-on-the-Walls,
between birth and 12 years of age. Although in this study
growth differences between the modern and medieval
samples already began at birth, and not just since adolescence, this was attributed to the worse living conditions
9
Fig. 5. Trends in male adult stature between the medieval
period and the late 20th century in Leiria, and between the
early and late 20th century in Lisbon. Leiria is represented by
the circles, which are connected by a broken line. Lisbon is represented by the squares, which are connected by a solid line.
of the industrial London compared to the earlier medieval
urban cities.
Results in this study show similar detrimental effects
on adolescent growth of increased urbanization of Lisbon, compared with Leiria and, in general, imply that
the early 20th century in Lisbon provided at least similarly unfavorable environmental conditions than that of
the late Middle Ages in Leiria, if not overall worse circumstances once children entered the labor market. This
relative depression in living conditions at the early 20th
century, compared with the medieval period, is also illustrated in Figure 5. In this figure, conscript male stature
from the Leiria and Lisbon areas in 1904 and 2000 are
shown, compared with the estimated statures from mean
male femur length of the medieval Leiria and the early
20th century Lisbon samples. Stature in this figure was
estimated from Mendonça’s (2000) male formulae. The
mean year at age 18 in the Lisbon sample (1931) and
the mid-point of the Leiria sample chronology (1382) are
used to plot the stature estimations. A remarkable
increase in conscript stature can be seen from the early
(1904) to the late 20th (2000) century and the stature
estimation for the Lisbon sample is what would be
expected given the birth dates of the this sample, the
general secular trend in Portugal, and the greater secular effect later in the century (Padez, 2003). On the other
hand, this figure clearly shows the reduced stature of
the Lisbon males in 1904 compared with the Leiria medieval males, and a further reduction of the Leiria males
also in 1904. This is an additional and strong indication
of the depressed living conditions of the early 20th century in Portugal compared with the medieval period.
These results suggest, indirectly, that it was industrialization and increased urbanization in the early 20th century, that had a detrimental effect on the growth of the
more modern children, more so than the supposedly miserable peasant living conditions of the medieval period.
In other words, the ‘‘Dark Ages’’ may not have been so
dark once we compare the overall living conditions
between these two periods and the two urban centers.
Indeed, the title of this paper could also have been
‘‘the not-so-prosperous industrial period in Portugal.’’
American Journal of Physical Anthropology
10
H.F.V. CARDOSO AND S. GARCIA
Although, there was no real industrial revolution in Portugal, the city of Lisbon supported important small
industries and a large service sector, which promoted an
increase in population density, where living conditions
for the working classes were frequently crowded, unsanitary, and offered increased risks of infection, malnutrition, probably not unlike the circumstances of medieval
Leiria, except perhaps in child labor practices which
may have placed Lisbon adolescents at greater risk of
undernutrition.
CONCLUSION
This study compared the growth status of late medieval children with that of early 20th century urban/industrial children from Portugal. Because the growth of children provide such a good index of the quality of the environment in which they live and, as consequence, of the
overall population, the results in this study strongly suggest similarly unfavorable environmental conditions in
early 20th century Lisbon compared with medieval Leiria. This stems from the fact that growth of medieval
children did not differ significantly from growth of modern children. However, because medieval adolescents
may have had more opportunities for catch-up growth,
since they had longer femora as adults; distinct child
labor practices in both periods may have caused a
decline in early 20th century children living conditions.
Although medieval Leiria and early 20th century Lisbon
may not have differed in the overall disease environment, early 20th century Lisbon provided a poorer environment for human growth during adolescence as a consequence of exhausting work being added to children’s
burdens of disease and poor diet, when they entered the
labor market. Although the lives of medieval children
may have been as difficult, they were not further deteriorated after puberty. The application of these hypotheses to the patterns of childhood and adolescent growth of
these medieval and late modern Portuguese children is
speculative, but even scarce documentary data seems to
correlate with higher rates of child labor, greater chronic
mild-to-moderate undernutrition, and generally unfavorable environment for growth in Lisbon compared with
Leiria, but only in the adolescent period.
ACKNOWLEDGMENTS
We would like to express our gratitude to the anonymous reviewers and to the editor for their comments and
suggestions, which helped to improve the paper significantly. We would also like to thank Dr. Barry Bogin’s
comments and corrections to an earlier version of this
paper and the late Dr. Shelley Saunders for providing us
the adult data from the Belleville skeletal sample.
Thanks to the Bocage Museum for institutional support
and the Leiria municipality for providing the opportunity to study the São Martinho sample.
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